Auchincloss, A. H. and Zerges, William and Perron, Karl and Girard-Bascou, Jacqueline and Rochaix, Jean-David
Characterization of Tbc2, a nucleus-encoded factor specifically required for translation of the chloroplast psbC mRNA in Chlamydomonas reinhardtii.
The Journal of Cell Biology, 157
- Published Version
Official URL: http://dx.doi.org/10.1083/jcb.200201060
Genetic analysis has revealed that the three nucleus-encoded factors Tbc1, Tbc2, and Tbc3 are involved in the translation of the chloroplast psbC mRNA of the eukaryotic green alga Chlamydomonas reinhardtii. In this study we report the isolation and phenotypic characterization of two new tbc2 mutant alleles and their use for cloning and characterizing the Tbc2 gene by genomic complementation. TBC2 encodes a protein of 1,115 residues containing nine copies of a novel degenerate 38–40 amino acid repeat with a quasiconserved PPPEW motif near its COOH-terminal end. The middle part of the Tbc2 protein displays partial amino acid sequence identity with Crp1, a protein from Zea mays that is implicated in the processing and translation of the chloroplast petA and petD RNAs. The Tbc2 protein is enriched in chloroplast stromal subfractions and is associated with a 400-kD protein complex that appears to play a role in the translation of specifically the psbC mRNA.
References:Bairoch, A., and R. Apweiler. 2000. The SWISS-PROT protein sequence database and its supplement TrEMBL. Nucleic Acids Res. 28:45–48.
Barkan, A., and M. Goldschmidt-Clermont. 2000. Participation of nuclear genes in chloroplast gene expression. Biochimie. 82:559–572.
Bennoun, P., A. Masson, and M. Delosme. 1980. A method for complementation analysis of nuclear and chloroplast mutants of photosynthesis in Chlamydomonas. Genetics. 95:39–47.
Bennoun, P., M. Spierer-Herz, J. Erickson, J. Girard-Bascou, Y. Pierre, M. Delsome, and J.-D. Rochaix. 1986. Characterization of photosystem II mutants of Chlamydomonas reinhardtii lacking the psbA gene. Plant Mol. Biol. 6:151–160.
Blatch, G.L., and M. Lassle. 1999. The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays. 21:932–939.
Boudreau, E., Y. Takahashi, C. Lemieux, M. Turmel, and J.-D. Rochaix. 1997. The chloroplast ycf3 and ycf4 open reading frames of Chlamydomonas reinhardtii are required for the accumulation of the photosystem I complex. EMBO J. 16:6095–6104.
Boudreau, E., J. Nickelsen, S.L. Lemaire, F. Ossenbühl, and J.-D. Rochaix. 2000. The Nac2 gene of Chlamydomonas encodes a chloroplast TPR-like protein involved in psbD mRNA stability. EMBO J. 19:3366–3376.
Chua, N.H., and P. Bennoun. 1975. Thylakoid membrane polypeptides of Chlamydomonas reinhardtii: wild-type and mutant strains deficient in photosystem II reaction center. Proc. Natl. Acad. Sci. USA. 72:2175–2179.
Church, G.M., and W. Gilbert. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA. 81:1991–1995.Abstract/FREE Full Text↵ Danon, A., and S.P. Mayfield. 1991. Light regulated translational activators: identification of chloroplast gene specific mRNA binding proteins. EMBO J. 10:3993–4001.
Das, A.K., P.W. Cohen, and D. Barford. 1998. The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein-protein interactions. EMBO J. 17:1192–1199.
Durrant, I. 1990. Light-based detection of biomolecules. Nature. 346:297–298.CrossRefMedline↵ Edwards, T.A., S.E. Pyle, R.P. Wharton, and A.K. Aggarwal. 2001. Structure of Pumilio reveals similarity between RNA and peptide binding motifs. Cell. 105:281–9.
Fisk, D.G., M.B. Walker, and A. Barkan. 1999. Molecular cloning of the maize gene crp1 reveals similarity between regulators of mitochondrial and chloroplast gene expression. EMBO J. 18:2621–2630.
Fong, C.L., A. Lentz, and S.P. Mayfield. 2000. Disulfide bond formation between RNA binding domains is used to regulate mRNA binding activity of the chloroplast poly(A)-binding protein. J. Biol. Chem. 275:8275–8278.
Franzen, L.G., J.D. Rochaix, and G. von Heijne. 1990. Chloroplast transit peptides from the green alga Chlamydomonas reinhardtii share features with both mitochondrial and higher plant chloroplast presequences. FEBS Lett. 260:165–168.
Goldschmidt-Clermont, M. 1998. Coordination of nuclear and chloroplast gene expression in plant cells. Int. Rev. Cytol. 177:115–180.
Goldschmidt-Clermont, M., J. Girard Bascou, Y. Choquet, and J.D. Rochaix. 1990. Trans-splicing mutants of Chlamydomonas reinhardtii. Mol. Gen. Genet. 223:417–425.
Gorman, D.S., and R.P. Levine. 1966. Cytochrome f and plastocyanin: their sequence in the photoelectric transport chain. Proc. Natl. Acad. Sci. USA. 54:1665–1669.
Groves, M.R., N. Hanlon, P. Turowski, B.A. Hemmings, and D. Barford. 1999. The structure of the protein phosphatase 2A PR65/A subunit reveals the conformation of its 15 tandemly repeated HEAT motifs. Cell. 96:99–110.
Harris, E.H. 1989. The Chlamydomonas Source Book: A Comprehensive Guide to Biology and Laboratory Use. Academic Press, San Diego. 780 pp.
Huber, A.H., W.J. Nelson, and W.I. Weis. 1997. Three-dimensional structure of the armadillo repeat region of β-catenin. Cell. 90:871–882.
Jenkins, B.D., and A. Barkan. 2001. Recruitment of a peptidyl-tRNA hydrolase as a facilitator of group II intron splicing in chloroplasts. EMBO J. 20:872–879.
Kim, J., and S.P. Mayfield. 1997. Protein disulfide isomerase as a regulator of chloroplast translational activation. Science. 278:1954–1957.
Kindle, K.L. 1990. High-frequency transformation of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA. 87:1228–1232.
Kuras, R., C. de Vitry, Y. Choquet, J. Girard-Bascou, D. Culler, S. Buschlen, S. Merchant, and F.A. Wollman. 1997. Molecular genetic identification of a pathway for heme binding to cytochrome b6. J. Biol. Chem. 272:32427–32435.
Lamb, J.R., S. Tugendreich, and P. Hieter. 1995. Tetratrico peptide repeat interactions: to TPR or not to TPR? Trends Biochem. Sci. 20:257–259.
Perron, K., M. Goldschmidt-Clermont, and J.D. Rochaix. 1999. A factor related to pseudouridine synthases is required for chloroplast group II intron trans-splicing in Chlamydomonas reinhardtii. EMBO J. 18:6481–6490.
Rattanachaikunsopon, P., C. Rosch, and M.R. Kuchka. 1999. Cloning and characterization of the nuclear AC115 gene of Chlamydomonas reinhardtii. Plant Mol. Biol. 39:1–10.
Rivier, C., M. Goldschmidt-Clermont, and J.D. Rochaix. 2001. Identification of an RNA-protein complex involved in chloroplast group II intron trans-splicing in Chlamydomonas reinhardtii. EMBO J. 20:1765–1773.
Rochaix, J.D. 2001. Posttranscriptional control of chloroplast gene expression from RNA to photosynthetic complex. Plant Physiol. 125:142–144.
Rochaix, J.D., M. Kuchka, S. Mayfield, M. Schirmer-Rahire, J. Girard-Bascou, and P. Bennoun. 1989. Nuclear and chloroplast mutations affect the synthesis or stability of the chloroplast psbC gene product in Chlamydomonas reinhardtii. EMBO J. 8:1013–1021.
Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
Schmidt, G.W., K.S. Matlin, and N.H. Chua. 1977. A rapid procedure for selective enrichment of photosynthetic electron transport mutants. Proc. Natl. Acad. Sci. USA. 74:610–614.
Sieburth, L.E., S. Berry-Lowe, and G. Schmidt. 1991. Chloroplast RNA stability in Chlamydomonas: rapid degradation of psbB and psbC transcripts in two nuclear mutants. Plant Cell. 3:175–189.
Small, I.D., and N. Peeters. 2000. The PPR motif—a TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 25:46–47.
Trebitsh, T., A. Levitan, A. Sofer, and A. Danon. 2000. Translation of chloroplast psbA mRNA is modulated in the light by counteracting oxidizing and reducing activities. Mol. Cell Biol. 20:1116–1123.
Trebitsh, T., E. Meiri, O. Ostersetzer, Z. Adam, and A. Danon. 2001. The protein disulfide isomerase-like RB60 is partitioned between stroma and thylakoids in Chlamydomonas reinhardtii chloroplasts. J. Biol. Chem. 276:4564–4569.
Vaistij, F.E., E. Boudreau, S.D. Lemaire, M. Goldschmidt-Clermont, and J.D. Rochaix. 2000. Characterization of Mbb1, a nucleus-encoded tetratricopeptide-like repeat protein required for expression of the chloroplast psbB/psbT/psbH gene cluster in Chlamydomonas reinhardtii. Proc. Natl. Acad Sci. USA. 97:14813–14818.
Wollman, F.A., L. Minai, and R. Nechushtai. 1999. The biogenesis and assembly of photosynthetic proteins in thylakoid membranes1. Biochim. Biophys. Acta. 1411:21–85.
Yohn, C.B., A. Cohen, A. Danon, and S.P. Mayfield. 1998. A poly(A) binding protein functions in the chloroplast as a message-specific translation factor. Proc. Natl. Acad. Sci. USA. 95:2238–2243.
Zerges, W., and J.D. Rochaix. 1994. The 5′ leader of a chloroplast mRNA mediates the translational requirements for two nucleus-encoded functions in Chlamydomonas reinhardtii. Mol. Cell Biol. 14:5268–5277.
Zerges, W., and J.D. Rochaix. 1998. Low density membranes are associated with RNA-binding proteins and thylakoids in the chloroplast of Chlamydomonas reinhardtii. J. Cell Biol. 140:101–110.
Zerges, W., J. Girard-Bascou, and J.D. Rochaix. 1997. Translation of the chloroplast psbC mRNA is controlled by interactions between its 5′ leader and the nuclear loci TBC1 and TBC3 in Chlamydomonas reinhardtii. Mol. Cell Biol. 17:3440–3448.
Zhang, H., P.L. Herman, and D.P. Weeks. 1994. Gene isolation through genomic complementation using an indexed library of Chlamydomonas reinhardtii DNA. Plant Mol. Biol. 24:663–672.
All items in Spectrum are protected by copyright, with all rights reserved. The use of items is governed by Spectrum's terms of access
Repository Staff Only: item control page